SEROTYPING AND RESISTANCE PROFILES OF S. ENTERICA
SEROTYPES AND ANTIMICROBIAL RESISTANCE OF SALMONELLA ENTERICA SSP IN CENTRAL THAILAND, 2001-2006 Pantip Sirichote1, Aroon Bangtrakulnonth2, Kanokwan Tianmanee1, Aekkawat Unahalekhaka1, Amonrat Oulai1, Patcharee Chittaphithakchai1, Wachirapa Kheowrod1 and Rene S Hendriksen3 1
Regional Medical Sciences Center, Samut Songkhram, Department of Medical Sciences, Ministry of Pubic Health, Nonthaburi, Thailand; 2S & A Reagents Lab, Lat Phrao, Bangkok, Thailand; 3WHO Collaborating Center for Antimicrobial Resistance in Food Borne Pathogens and EU Community Reference Laboratory for Antimicrobial Resistance, National Food Institute, Technical University of Denmark, Kgs Lyngby, Denmark Abstract. This study was carried out to elucidate the epidemiological trends and antimicrobial susceptibilities against Salmonella serovars among Thai patients and asymptomatic carriers during 2001-2006 in central Thailand. A total of 1,401 human and 260 non-human isolates from various sources were included. The isolates were characterized using serotyping and antimicrobial susceptibility testing. The most common serovars in patients submitting stool samples were S. Weltevreden, S. Stanley, S. Anatum, and S. Rissen. Significantly higher odds ratios were observed in blood samples versus stool sample for S. Choleraesuis, S. Enteritidis, S. Typhimurium, and S. Typhi. Children under five years old suffered the most frequently from gastroenteritis. The patients most commonly infected with an invasive serovar were children and people from 26 to 55 years of age. Antimicrobial susceptibility data revealed that S. Schwarzengrund, S. Choleraesuis, S. Anatum, S. Stanley, S. Rissen, and S. Typhimurium were the most resistant serovars observed. The invasive serovar, S. Choleraesuis was resistant to cefotaxime and norfloxacin. Antimicrobial resistance to cefotaxime, was observed in S. Agona, S. Rissen, S. Typhimurium, S. Anatum, and S. Weltevreden. An alarmingly high frequency of resistance to third generation cephalosporins was observed. We recommend Thai authorities take action in order to prevent spread of resistant S. Choleraesuis and other serovars among animals and humans by enforcing a more strict policy on the use of antimicrobials in food animals. Key words: Salmonella enterica, serotype, antimicrobial resistance, Thailand
INTRODUCTION Correspondence: Rene S Hendriksen, National Food Institute, Technical University of Denmark, Kemitorvet, DK-2800 Kgs Lyngby, Denmark. Tel: +45 35 88 60 00; Fax: +45 35 88 63 41 E-mail:
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Salmonella enterica is a common cause of human gastroenteritis and bacteremia worldwide ( Schlundt et al, 2004; Voetsch et al, 2004; Hendriksen et al, 2009; Morpeth et al, 2009). A wide variety of animals, par1405
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ticularly food animals, have been identified as reservoirs for non-Typhi Salmonella (Guard-Petter, 2001; Bangtrakulnonth et al, 2004; Vindigni et al, 2007). Although approximately 2,600 serovars of Salmonella enterica have been identified, most human infections are caused by a limited number of serovars and in general these infections are self limited. Some Salmonella serovars, such as Salmonella enterica serovar Choleraesuis, S. Dublin, S. Panama, S. Heidelberg, and S. Enteritidis, have a propensity to cause extra-intestinal infections in humans. When compared to other serovars of non-Typhi Salmonella, infections with these serovars are associated with higher rates of bacteremia, meningitis, and mortality (Helms et al, 2003; Chiu et al, 2004; Helms et al, 2006; Jones et al, 2008; Hendriksen et al, 2009). For patients with severe salmonellosis, antimicrobial chemotherapy may be lifesaving. Due to the increasing prevalence of fluorquinolone resistance and the increasingly use of third generation cephalosporins to treat Salmonella infections in humans (Hohmann, 2001; Grohskopf et al, 2005; Kulwichit et al, 2007; Lee et al, 2009), these drugs have been designated as critically important for human health by the World Health Organization (Collignon et al, 2009). In developed countries, S. Typhimurium and S. Enteritidis are the most common causes of human salmonellosis, but other serovars have been reported to be more prevalent in specific regions and even within countries (Herikstad et al, 1997; Bangtrakulnonth et al, 2004; Galanis et al, 2006; Hendriksen et al, 2009; Lee et al, 2009). Laboratory surveillance of Salmonella serovars in humans, animals and food products is crucial for understanding the epidemiology of the different serovars and
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spread from these reservoirs to people. Numerous publications have addressed the emergence of different Salmonella serovars in Thailand, providing additional knowledge of the epidemiology and reservoirs accounting for infections in humans (Aarestrup et al, 2003; Bangtrakulnonth et al, 2004; Archambault et al, 2006; Aarestrup et al, 2007; Hendriksen et al, 2008, 2009). A retrospective observational study was conducted to elucidate the epidemiological trends and antimicrobial susceptibilities of the most common Salmonella serovars among Thai patients during 2001-2006 in central Thailand. This study also assessed which infected age groups were associated with gastrointestinal salmonellosis and bacteremia using descriptive data. The data gained in this study may assist policy makers to develop serovar specific interventions to minimize the burden of the most common Salmonella serovars in Thailand, and to enforce a more restrictive policy regarding the use of antimicrobials for primary production. MATERIALS AND METHODS Bacterial isolates
From August 2001 to March 2006, a total of 1,401 Salmonella isolates obtained from humans and 260 isolates from 209 various non-human sources were serotyped and the antimicrobial susceptibilities were determined at the Regional Medical Sciences Center, Samut Songkhram, Thailand. The human isolates (patient stool=922 specimens, patient blood=136 specimens, and stool from asymptomatic carriers=343 specimens) originated from 8 sentinel hospitals in central Thailand. The asymptomatic carriers were mainly food handlers working in food producing factories; stool
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SEROTYPING AND RESISTANCE PROFILES OF S. ENTERICA
samples were collected during routinely screening for gastrointestinal diseases. Several Salmonella serovars (N) were isolated from non-human samples (n). The isolates originating from non-human sources were obtained from fresh retail meat [pork (N=83/n=65), seafood (N=20/ n=16), chicken (N=44/n=30), beef (N=14/ n=12), freshwater fish and prawn (N=2/ n=2)], ready to eat food (N=6/n=6), vegetables (N=3/n=3), beverages (N=1/n=1), fresh water (N=8/n=7), waste water from raw animal products (N=3/n=3), ice (N=2/ n=2) and swabs from unidentified sources (N=74/n=62). The isolates were identified using approved internationally recognised standard procedures as previously described (Bangtrakulnonth et al, 2004). Statistical analysis
SAS version 9.1.3 (SAS Institute, Cary, NC) was used to assess the association of specific serovars present in patients submitting blood samples, patients submitting stool samples and asymptomatic carriers submitting stool samples. The significance level was set at p 8 3 5 7 7 6 5 6 2 2 1 3 4 4 1 41.6-213.7), S. Typhi (OR 57.6; 95% Age group (years) CI 7.1-464.0), S. Enteritidis (OR Fig 1–Distribution of age groups among patients submit5.4; 95% CI 3.3-8.9), and S. ting stool and blood samples during 2001-2006. Typhimurium (OR 3.5; 95% CI 1.96.2). S. Stanley, S. Weltevreden, and S. gastroenteritis during 2001-2006, 263 were Anatum were more common in stool than in children 50 cases (Fig 1). The distribution of patients with invasive serovars Only 5 of the 10 most common serovars differed from the distribution of patients were present in both patients and healthy suffering from gastrointestinal salmonelcarriers in stool: S. Stanley, S. Anatum, losis. Patients 60 years old. Hendriksen et al (2009) also suggested S. Anatum, S. Enteritidis, and S. Weltevreden caused age specific, infections which mainly affected people >6 years old, while S. Stanley, S. Panama, and S. I (1),4,(5),12:i:- caused infections mainly in children
